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Advanced Online Publication Chinaxiv:201908.00095V1 ChinaXiv合作期刊 古 脊 椎 动 物 学 报 VERTEBRATA PALASIATICA DOI: 10.19615/j.cnki.1000-3118.190823 First report of immature feathers in juvenile enantiornithines from the Early Cretaceous Jehol avifauna Jingmai K. O’CONNOR1,2 Amanda FALK3 WANG Min1,2 ZHENG Xiao-Ting4,5 (1 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences Beijing 100044, China [email protected]; [email protected]) (2 CAS Center for Excellence in Life and Paleoenvironment Beijing 100044, China) (3 Centre College 600 W. Walnut St. Danville, Kentucky 40422, USA) (4 Institute of Geology and Paleontology, Linyi University Linyi, Shandong 276000, China) (5 Shandong Tianyu Museum of Nature Pingyi, Shandong 273300, China) AdvancedAbstract Molting—the process replacing one plumage with another—is a critically important biological function in Aves. This process annually replaces the feather coat, damaged by normal wear and tear, produces ontogenetic changes in feathering, and produces alternate breeding plumages associated with reproductive activity in adults. Immature, growing feathers are encased in a keratinous sheath, giving them a narrow, tubular, and featureless appearance. The complete loss of the sheath indicates the feather is mature. Despite the wealth of integumentary data published from the Jehol Biota, immature feathers have never been definitively reported, although they may potentiallyonline be preserved in a juvenile specimen of the non-avian oviraptorosaur theropod dinosaur Similicaudipteryx from the 120 Ma Jiufotang Formation. A developing feather has been reported in a 99 Ma enantiornithine neonate preserved in Burmese amber, in which three-dimensional preservation makes interpretations of integumentary structures more straightforward. Here we report on probable immature featherspublication in four juvenile enantiornithines (Aves: Ornithothoraces) from the Jehol Group. As observed in developing feathers in extant birds, the purported immature fossil feathers appear proximally narrow and featureless with barbs protruding only distally. Based on our observations, we suggest that similar-appearing feather structures preserved on the manus and tibiotarsus in the holotype of the enantiornithine chinaXiv:201908.00095v1 Cruralispennia multidonta may alternatively be interpreted as immature feathers. The presence of immature feathers in combination with sexually dimorphic ornamental feathers in juvenile enantiornithines suggests the complex molting patterns of Neornithes, in which such ornaments only appear after several years (following several molts) when reproductive activity is achieved, are limited to a subset of crownward avians. Keywords Mesozoic, Jehol Biota, Aves, pin feather, plumage, molt Citation O’Connor J K, Falk A, Wang M et al., in press. First report of immature feathers in juvenile enantiornithines from the Early Cretaceous Jehol avifauna. Vertebrata PalAsiatica, DOI: 10.19615/j.cnki.1000-3118.190823 国家自然科学基金(批准号：41688103, 41372014)资助。 收稿日期：2019-04-15 ChinaXiv合作期刊 2 1 Introduction Most data concerning the integument of the non-neornithine Pennaraptora – the clade that includes all dinosaurs (including birds) with pennaceous feathers, comes from the Middle- Upper Jurassic Yanliao and Lower Cretaceous Jehol lagerstatten in northeastern China (Zhang et al., 2006; Sullivan et al., 2017). Thousands of specimens have been collected from these volcanolacustrine deposits, hundreds of which preserve traces of integument that are typically rare in the fossil record. These specimens have provided direct evidence of plumage patterns (Zheng et al., 2017; Li et al., 2018) and melanosome-based coloration (Zhang et al., 2010), revealed extinct feather morphotypes (Zhang et al., 2006; O’Connor et al., 2012), and shed Advancedlight on the evolution of individual feather tracts (e.g., crus, tail) (Zheng et al., 2013; Wang et al., 2014; O’Connor and Chang, 2015). Despite this wealth of data, many gaps remain in our understanding. The preserved plumage cannot be considered complete in any specimen, and the two-dimensional preservation of most specimens makes preserved traces difficult to interpret with certainty. Ontogenetic changes in plumage, non-melanosome based coloration, the location of apteryia and much more remain largely unexplored. Most modern birds begin with a natal plumage that is replaced, through molting, with a series of plumages (juvenal, pre-basic)online until the first basic plumage of the subadult is acquired, and then go through another series of plumages (second basic, third basic) until the definitive basic plumage of the mature adult appears, which may take up to eight years in some species (Lovette and Fitzpatrick, 2004). As a new feather forms it pushes out the older feather so that molting and new feather formation are essentially a singlepublication process (Lucas and Stettenheim, 1972). Immature (developing) feathers are readily identifiable as they emerge, being encased in a tubular waxy sheath, which is completely removed through preening after the feather cells have died and dried allowing the curled feather vanes to unfurl into a planar structure revealing their pennaceous morphology (Lovette and Fitzpatrick, 2004). The sheath is a keratinized chinaXiv:201908.00095v1 epithelial tube that forms separately from the feather in the outer epidermal collar (Murphy and King, 1986; Lovette and Fitzpatrick, 2004). The presence of the sheath obscures observation of the feather structure within and gives the feather a narrow and solid appearance; the rachis and barbs are only visible where the sheath has been removed (Figs. 1, 2). Molting occurs in living birds for two reasons: during early ontogeny exchanging natal, juvenal, pre-basic, and non- definitive basic plumages; and as adults in the definitive molt cycle associated with an annual renewal of the basic plumage and seasonally associated with an alternate plumage related to breeding and more rarely, a supplemental plumage that provides camouflage (Amadon, 1966; Lucas and Stettenheim, 1972; Lovette and Fitzpatrick, 2004). If a bird goes straight from the juvenal to the definitive basic plumage, the molt strategy is considered simple. If these two plumages are separated by additional molts (first basic, etc.), the molt strategy is termed complex (Lovette and Fitzpatrick, 2004). When a feather is damaged it is not replaced until the next molt. However, immature feathers may occur outside these ontogenetic or annual ChinaXiv合作期刊 O’Connor et al. - First report of immature feathers in juvenile enantiornithines 3 molt cycles if a feather is lost entirely in which case it is immediately replaced; this feather replacement is not considered a molt (Lovette and Fitzpatrick, 2004). Feather emergence has not been convincingly documented in any avian specimen from the rich Jehol Biota. However, immature feathers have been proposed to be present Advanced online publication chinaXiv:201908.00095v1 Fig. 1 Immature feathers in juvenile neornithines A. late immature remiges in Pelecanus occidentalis LACM 86193; B. mid to late immature remiges in Otus asio LACM 100682; C. mid to late immature remiges in Turdus migratorius LACM 100338; D–F. mid immature contour feathers in Tyto alba LACM 100815 (nestling). Note tubular (‘ribbon-like’ in compression fossils) appearance of the proximally sheathed portions of the developing feathers Abbreviations: fv. feather vane (exposed distal to the proximal developing portion of the feather still encased in the waxy sheath); sh. waxy sheath ChinaXiv合作期刊 4 in a juvenile specimen of the oviraptorosaur (Maniraptora: Pennaraptora) Similicaudipteryx (Fig. 3) (Prum, 2010), although this identification is not without controversy (Prum, 2010; Xu et al., 2010a, b). The unusual feather traces preserved in Similicaudipteryx STM 4-1 were originally interpreted as representing a distinct feather morphotype, the so-called ‘proximally ribbon-like pennaceous feathers’ (PRPFs) (Xu et al., 2010a, b). Interpreting two-dimensional Advanced fossilized traces is notoriously difficult and with only a single juvenile specimen of Similicaudipteryx available, it is difficult to weigh these two competing hypotheses. However, in this case disagreement may be exacerbated by confusing terminologies. Prum (2010) referred to the immature feathers in STM Fig. 2 Illustration of the stages inonline feather 4-1 as pin-feathers. This hypothesis was rejected development A. pin feather, early immature stage; by Xu et al. (2010b) based on the large size B. blood-quill, mid-immature stage; of the feather structures in question. Although C. late immature stage; D. mature feather widely used to refer to all immature feathers (Lovette and Fitzpatrick, 2004), the term pin-feather technicallypublication refers only to the early stages of feather growth (early immature), when the developing feather is short and entirely encased in its sheath (and thus resembling a pin) (Lucas and Stettenheim, 1972) (Fig. 2A). At this stage the feather would most likely not be visible, blocked from view by other surrounding feathers, unless it belonged to the first incoming natal plumage of an altricial chick (born chinaXiv:201908.00095v1 naked) or a complete molt (all feathers molting at the same time, rare in Neornithes) (Lovette and Fitzpatrick, 2004). As the feather continues to elongate it becomes a blood quill, the mid-immature stage (Figs. 1D–F, 2B). The name derives from the richly vascularized
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